key: cord-0883833-q4gij6fm
authors: Zhao, Alice; Dangerfield, Derek T.; Nunn, Amy; Patel, Rupa; Farley, Jason E.; Ugoji, Chinenye C.; Dean, Lorraine T.
title: Pharmacy-Based Interventions to Increase Use of HIV Pre-exposure Prophylaxis in the United States: A Scoping Review
date: 2021-10-20
journal: AIDS Behav
DOI: 10.1007/s10461-021-03494-4
sha: d1478ab9085cc60a35c236c0875c49c4128f9d76
doc_id: 883833
cord_uid: q4gij6fm

HIV pre-exposure prophylaxis (PrEP) remains underutilized in the U.S. Since greater than 85% of PrEP prescriptions are filled at commercial pharmacies, pharmacists are uniquely positioned to increase PrEP use. This scoping review explores pharmacy-based initiatives to increase PrEP use. We searched PubMed, PsycINFO, CINAHL, and Scopus for peer-reviewed studies on pharmacist-led interventions to increase PrEP use or pharmacy-based PrEP initiatives. Forty-nine articles were included in this review. Overall, studies demonstrated that patients expressed strong support for pharmacist prescription of PrEP. Three intervention designs compared changes in PrEP initiation or knowledge pre- and post-intervention. Commentary/review studies recommended PrEP training for pharmacists, policy changes to support pharmacist screening for HIV and PrEP prescription, and telemedicine to increase prescriptions. Pharmacists could play key roles in improving PrEP use in the U.S. Studies that assess improvements in PrEP use after interventions such as PrEP prescription, PrEP-specific training, and adherence monitoring by pharmacists are needed.

Oral pre-exposure prophylaxis (PrEP) for HIV, Truvada® (emtricitabine, tenofovir disoproxil fumarate) and Descovy® (emtricitabine and tenofovir alafenamide), can reduce HIV acquisition risk from sex by 92-99% when used daily [1] [2] [3] [4] [5] [6] . Although PrEP use is generally increasing in the United States, with over 50,000 new PrEP users in 2018 [7] , only a small proportion of high-risk populations with CDC risk indicators have initiated PrEP [8] [9] [10] . Uptake and adherence are disproportionately low among individuals clinically indicated for PrEP and in subpopulations such as sexual minority men, transwomen, cisgender women, and sex workers [11] [12] [13] . Disparities in PrEP initiation by age, race, sex, and geography are widening in the U.S. [14] .

Despite increased vulnerability to HIV acquisition, only ~ 1% of clinically indicated African Americans and 3% of clinically indicated Hispanics/Latinos were actually prescribed PrEP, compared to 14% of clinically indicated Whites [15, 16] . Additionally, people in the U.S. South have a lower rate of PrEP prescription to HIV incidence than other U.S. region [8] . Regarding sex distributions, females have a lower ratio of new PrEP prescriptions to new HIV diagnoses compared to males [7, 17, 18] . Among those who initiate PrEP, adherence is low [19] [20] [21] [22] [23] [24] [25] . Only 50-60% of patients are retained in PrEP care after 1 year [19, 26] . Barriers to PrEP initiation and adherence include low awareness, limited knowledge, and poor perceptions of PrEP by patients and providers [27, 28] . Further, limited access due to transportation, high healthcare and copay costs, and disparities in provider prescription, all present a crucial need to expand PrEP access. Pharmacies play important roles in PrEP acquisition and adherence by facilitating access to prescriptions [29, 30] .

There are approximately 67,000 retail pharmacies in the U.S., many of which offer home-delivery services, drivethrough services, and multilingual staff [29] ; 85-90% of PrEP prescriptions are filled at commercial pharmacies [31] . Pharmacies could bring the U.S. closer to plans for Ending the HIV Epidemic in the U.S. (EHE) by 2030 [32] . Pharmacists historically have been able to order testing and prescribe medications under: (1) collaborative practice agreements (CPAs); and (2) state laws that permit prescribing for pharmacists; however, currently, California, Oregon, and Colorado are the only U.S. states to legalize the authority of pharmacists to prescribe and dispense PrEP independently [33, 34] . Most states have legalized the authority of pharmacists to prescribe and dispense PrEP in collaboration with other healthcare providers. More states and cities have increased discussions regarding the prescriptive authority of PrEP to pharmacists, and the Veterans Health Administration (VHA) has nationally approved pharmacist prescription of numerous medications [34, 35] . Pharmacists could facilitate PrEP uptake and adherence through consultations with and HIV screening for interested individuals, point-ofcare testing for HIV and other sexually transmitted infections (STIs), PrEP prescriptions, and PrEP adherence counseling. Pharmacy-based interventions such as refill reminders and adherence counseling have improved medication adherence to antiretroviral therapy regimens among people living with HIV [36] [37] [38] . Although interventions that integrate pharmacists into the PrEP care continuum are increasing [39, 40] , information related to pharmacy-based PrEP interventions is limited.

To fill this gap, the purpose of this scoping review is to (1) review current evidence regarding attitudes toward PrEP and pharmacy-based interventions to increase PrEP initiation and adherence; (2) summarize findings from existing pharmacy-based PrEP interventions; and (3) identify best practices from commentaries and reviews of pharmacybased PrEP interventions. Reviewing and synthesizing existing models for pharmacy-based PrEP interventions could provide more insight into ways to increase PrEP initiation and adherence in the U.S. Findings of this study could be used to implement pharmacy-based interventions designed to increase PrEP initiation and adherence in the U.S.

We examined research activities, summarized findings, and consolidated recommendations in the literature concerning pharmacy-based PrEP interventions. We used a 5-step approach that included the following procedures: (1) identifying the research question (i.e., what is stated in the current literature on pharmacy-based PrEP interventions), (2) identifying the relevant studies, (3) study selection, (4) presenting the data, and (5) collating the results [41] . Consistent with the goals of a scoping review, selected studies were synthesized, and gaps in existing literature were identified [41, 42] .

We searched within four databases: PubMed, PsycINFO, CINAHL (Cumulative Index to Nursing and Allied Health Literature), and Scopus. To identify sources concerning HIV within PubMed, we used search terms such as "HIV*" OR "Anti-HIV Agents*" OR "HIV infections*" OR "HIV/AIDS" OR "Acquired Immunodeficiency Syndrome." The terms "Pre-Exposure Prophylaxis*" OR "PrEP" were searched to focus on PrEP specifically. Additionally, sources including data on pharmacists and/or pharmacies were captured using "pharmacy*" OR "pharmacies*" OR "pharmacy residencies*" OR "pharmacy service, hospital*" OR "community pharmacy services*" OR "evidence-based pharmacy practice*" OR "pharmaceutical services*" OR "pharmacist*" as terms. To find articles referencing pharmacists' ongoing or potential roles in PrEP initiation, terms such as "HIV Testing" OR "HIV Diagnose" OR "treatment adherence and compliance*" OR "medication adherence*" OR "patient compliance" OR "counsel" OR "monitor" were used. These search terms were modified as necessary when collecting sources from various databases. Boolean logic and MeSH terms were both used to maximize candidate articles. Additionally, a manual search was conducted within the references of articles emerging from the search; these sources were included in the subsequent title and abstract reviews if appropriate. These search strategies resulted in a total of 916 articles. All data searching was conducted by one reviewer.

Articles were selected if they met the following criteria: (1) published in a peer-reviewed journal between January 1, 2012 and June 11, 2021 (2012 demarcates the year that the U.S. Food and Drug Administration first approved PrEP [43] ); (2) focused primarily on PrEP in the article and presented data on the potential impact of pharmacies on PrEP acquisition and/or adherence; (3) included data and/or commentary on individuals eligible for PrEP or focused on PrEP administration or counseling by pharmacists; (4) conducted in the United States (Fig. 1 ).

After potential articles were collected, titles and abstracts were reviewed for relevance. We excluded candidates using the specified criteria, then subsequently conducted a full text review. Selected studies were divided into two categories upon acceptance: empirical studies, which consisted of sources containing primary observational data, and commentaries or reviews, which provided recommendations for PrEP-related interventions. Screening was conducted by two reviewers (AZ and LTD). To visualize the geographic locations where pharmacist knowledge of and familiarity with PrEP had been assessed, where pharmacy-based PrEP interventions have been implemented, and in which states PrEP prescriptive authority for pharmacists have been legalized, a map of the U.S. was created using Notability by Ginger Labs. State and regional percentages represent those of cohorts utilized in the included studies and do not necessarily reflect state-wide and regionwide data. The grid pattern represents states that have legalized independent pharmacist PrEP prescriptive authority as of June 2021. Percentages listed for Nebraska and Iowa reflect a study in which the data from each state were not disaggregated. Stars represent areas in which pharmacistled PrEP interventions have been implemented. HIV cases per 100,000 residents of respective state and PrEP users per 100,000 residents of respective state were listed in the image.

The initial database searching yielded a total of 916 studies. After de-duplication, the remaining 727 studies were screened based on title and abstract, resulting in the exclusion of 667 articles. The most common reasons for exclusion at this stage were that the title and/or abstract did not meet the focus criteria (n = 551) or that the study was not conducted in the U.S. (n = 110). The remaining 60 articles were retrieved for full text review, and 11 were excluded because they did not include relevant data or did not focus on pharmacies or pharmacists. Forty-nine studies met the specified inclusion criteria (Fig. 1 ).

Twenty-four empirical studies concerning pharmacist and patient perceptions of PrEP were identified ( Table 1 ). The sample size of such studies ranged from 9 [44] to 7148 [45] . Fourteen studies contained primary observational data concerning practicing pharmacists' and Doctor of Pharmacy (PharmD) students' knowledge, perceptions, and attitudes of pharmacy-based PrEP interventions [44, [46] [47] [48] [49] [50] [51] [52] [53] [54] [55] . Pharmacists and/or pharmacy students from all four of the U.S. Census Bureau regions were represented. Eight studies measured practicing pharmacist knowledge of PrEP, and pharmacist familiarity with PrEP and CDC guidelines for PrEP eligibility varied across different regions of the U.S [44, [47] [48] [49] [50] [56] [57] [58] . Five studies measured proportions of pharmacists with familiarity on PrEP and/or the CDC guidelines for PrEP; familiarity ranged from 42% in Nebraska and Iowa to 91% in New York [47, 56] . Additionally, two other studies found that pharmacists with more years of experience were less likely to be familiar with PrEP, while pharmacists with less than 10 years of experience had the highest PrEP knowledge and intention to counsel [47, 51] . Six studies examined PrEP awareness among pharmacy students, reporting rates of PrEP awareness of up to 97.7% among final year PharmD students [53] .

Eleven studies contained data concerning patient experiences with or attitudes toward PrEP pickup or prescription in pharmacies [45, 46, [59] [60] [61] [62] [63] [64] [65] [66] [67] . Ten of these studies targeted patients of high-risk populations, such as people who inject drugs and MSM, who were seeking to initiate PrEP. Reported barriers among these populations concerning PrEP delivery in pharmacies included a lack of medication availability, difficulty with mail refills, misinformation about medication cost, and privacy concerns [45, 46, [59] [60] [61] [62] [64] [65] [66] [67] . Two other studies targeted broader populations to collect general patient perspectives on the prescriptive authority of pharmacists. The first was a qualitative study, which examined the perceptions of PrEP delivery in pharmacies among MSM residing in Atlanta who were not necessarily interested in initiating PrEP [46] . Patients expressed strong support for future PrEP prescription and screening. In a second study on patients attending a grocery-chain pharmacy who were not necessarily eligible for or aware of PrEP, most patients reported no concerns regarding pharmacist prescription of PrEP [63] . One qualitative study, which included cisgender women, focused specifically on their attitudes toward long-acting injectable PrEP [65] .

Nine studies described the implementation of PrEP interventions within pharmacies (Table 2) . Despite consistent data suggesting the clinical benefit of PrEP since 2007, the first studies of PrEP interventions at pharmacies were not published until 2018. In these studies, community or hospital pharmacists were incorporated into a PrEP program. Only three of such interventions included a control group [68] ; the remaining studies evaluated newly implemented programs without comparison data. The most common intervention activity was pharmacist prescription of PrEP [69] [70] [71] [72] [73] [74] , which was well-received by patients [70] . Other activities included pharmacist facilitation of PrEP initiation via remote or telephone consultations with patients interested in PrEP [69, 71] . Four studies were designed to initiate PrEP among eligible participants, achieving successful PrEP initiation among a range of 54%-100% of participants [69] [70] [71] [72] 74] . A separate study, which focused on retention, employed a PrEP Navigation (PN) tool to minimize the number of days between PrEP prescription and pickup, ultimately shortening this interval by 1.42 days [68] . Additionally, two studies piloted programs that allowed for pharmacists to provide PrEP and HIV prevention curriculum for both undergraduate and graduate students [75, 76] .

16 commentaries and reviews were included based on eligibility criteria (Table 3) . These studies, which contained specific recommendations for future PrEP-related interventions within pharmacies, were published between the years 2012 and 2021. Twelve of the included commentaries and reviews recommended greater collaboration between pharmacists and providers [35, 40, [77] [78] [79] [80] [81] [82] [83] [84] [85] . Ten of the studies highlighted the utility of pharmacists performing HIV screening in order to identify HIV-negative individuals potentially eligible for PrEP [35, 78, 80, [82] [83] [84] [85] [86] [87] [88] . Two studies suggested the formation of Collaborative Practice Agreements (CPAs) that allow for the initiation and monitoring of PrEP by pharmacists [35, 82] . Additionally, two other studies suggested the formation of a Collaborative Drug Therapy Agreement (CDTA) that may similarly expand the scope of pharmacy practice to the prescription, modification, or discontinuation of PrEP [40, 80] . Such agreements would require the advocacy of policy changes that expand pharmacists' scope of practice in certain states [35] . Another common theme was the need to train pharmacists to properly provide patients with PrEP adherence counseling, sexual health counseling, and adverse side effect screening [77, 80, 82, [89] [90] [91] .

This scoping review collected existing literature on the growing potential of greater pharmacist involvement in PrEP delivery in the U.S. Studies that measured pharmacist counseling intentions and willingness to provide PrEP services noted a positive association between PrEP familiarity and counseling or prescribing intentions [46-48, 51, 56, 63] . Few studies explored pharmacist PrEP familiarity qualitatively, and there was a lack of longitudinal data displaying changes in knowledge and attitudes over time. Within studies investigating patient attitudes toward pharmacist prescriptive authority, most patients expressed support for greater pharmacist involvement in PrEP prescription and HIV screening. Prior to pharmacist involvement in PrEP prescription and HIV screening, further data are needed to determine areas in which pharmacists need comprehensive PrEP training. Studies measuring pharmacist knowledge of or familiarity with PrEP were concentrated in the Midwest U.S., which includes states with the lowest HIV prevalence. There were no studies based in the Western U.S., and few studies based in the South or Northeast regions (Fig. 2) . This could suggest incongruence between where PrEP is most needed and • 95% of participants were MSM • 100% of participants received a same-day PrEP prescription

• 33% of participants were referred for sameday PrEP filled a prescription and were properly linked to PrEP care where pharmacists are likely to be familiar with PrEP [57] . This finding could also suggest that pharmacists in areas with high HIV rates are already familiar with PrEP, indicating a more critical need for evaluation of pharmacist knowledge of PrEP in other U.S. regions. Given that seven studies highlighted an increased need for PrEP education among pharmacists [46] [47] [48] [49] [50] [51] 56] , PrEP education is still needed for pharmacists in order for future interventions to be properly implemented. Training, especially in non-specialty pharmacies, may aid in pharmacist interventions targeting PrEP. These trainings should address how to establish trusting relationships with patients and how to improve pharmacist comfort with discussing patients' sexual practices. For future pharmacists currently receiving PharmD curriculum, studies showed increasing integration of PrEP education into PharmD programs, providing data from all four regions of the U.S. [57] . No qualitative or longitudinal studies measured pharmacy student knowledge of or attitudes toward PrEP. However, in the included cross-sectional studies, significantly higher proportions of pharmacy students reported PrEP training compared to practicing pharmacists. This may explain the fact that pharmacists with fewer years of experience had a more comprehensive knowledge of PrEP and a higher intention to counsel. Additionally, because PharmD programs in the Northeast region have the most comprehensive PrEP education, this underscores the need to increase pharmacist PrEP training in other regions of the U.S., even in regions with a lower prevalence of HIV than the Northeast. PrEP training should be directly targeted toward more experienced pharmacists, as well as integrated into the core curriculum of pharmacy education; such new curricula may be piloted by practicing pharmacists.

Few studies investigated the implementation of PrEP interventions within pharmacies. Pharmacist-led PrEP programs that allow pharmacists to prescribe PrEP under a CPA show promise for PrEP initiation [70] . One of the included studies piloted a PrEP-focused curriculum led by pharmacists in California; however, no studies measured PrEP prescription by pharmacists in California, the first state in which autonomous pharmacist prescription of PrEP became legal [33] . Of the included intervention studies, most interventions opted for a program evaluation model, rather than a control group that would enable measurement of how much a pharmacy-based intervention might increase PrEP use. Greater comparison data are needed in future studies to assess change in PrEP use and adherence among postand pre-intervention groups, especially those that include pharmacist screening of eligible individuals and prescriptive authority of PrEP. Methods like difference-in-difference analysis might be used to compare changes in PrEP usage pre-and post-California's policy intervention compared with other states. Recently passed legislation in Colorado and Oregon offer further opportunities for study [92] [93] [94] . Pharmacy-based PrEP programs should consider integrating a comprehensive sexual health program inclusive of routine HIV/STI testing. Diagnosis and treatment of STIs should be considered as part of a pharmacy-based PrEP program; however, scope of practice laws could impact what services might be included in these interventions. Given the low trustworthiness in healthcare providers reported by Black and Latino MSM and its negative impact on PrEP uptake among these populations, having community pharmacists encourage PrEP use could be a more practical and approachable model that also reduces PrEP inequities [95, 96] . Thus, while many patients largely supported the idea of pharmacist prescription of PrEP, further studies are needed to assess attitudes of PrEP-eligible Black and Latinx MSM, who are disproportionately impacted by HIV infection within the U.S. The integration of pharmacists into the PrEP care continuum may increase the accessibility of PrEP among hard-to-reach populations that may be hesitant to use STI clinics or ask clinicians about PrEP. As such, the offer of HIV and STI testing by pharmacies is an immediate step that could be taken to generate demand and/or document the need for PrEP in a given pharmacy catchment area.

Structural and patient barriers to the incorporation of pharmacists into the PrEP continuum of care must be addressed prior to implementation. Structural barriers may include point-of-care testing for HIV diagnosis, suboptimal comfortability performing PrEP-related clinical activities, and issues with patient retention in PrEP care [44, 52, 69, 71] . Although community pharmacists are typically accessible to patients, difficulties in long-term retention still remain. Studies reporting clinics sites led by physicians measured that 57% and 30% of patients who initiated PrEP remain engaged in the PrEP continuum of care at 6 months and 12 months, respectively [19, 26] . Similar studies concerning pharmacist-led programs measured retention at 6 months and 12 months to be 61% and 28%, respectively [71] . Patient barriers may include confusion about insurance coverage and cost, privacy issues, as well as concerns about side effects of medication [60, 61, 68, 76] .

There are limitations to this scoping review. Due to the nature of this scoping review, this study did not assess the quality of selected studies, but rather collected existing data and knowledge concerning pharmacy-based PrEP interventions [41, 42] . This review may not have included all studies related to the selected topic; studies of pharmacy-based claims were not included. Although pharmacy claims could provide metrics for PrEP persistence, we did not consider claims analyses in this scoping review. Studies conducted outside of the U.S., as well as any non-English literature, were also omitted due to the unique structure of the U.S. pharmacy system. Consequently, it is possible that other studies covered this topic but were not included in this scoping review. However, of sources extracted from the six major databases previously listed, we believe that the depth of our search provides a comprehensive assessment of data related to pharmacy-based PrEP interventions. 

This scoping review provides evidence that an increasing number of studies are suggesting to expand the role of pharmacists in PrEP initiation and retention in care. High patient acceptance of pharmacy-based PrEP intervention is a strong foundation for the expansion of pharmacy-based PrEP interventions. However, the studies that implemented novel interventions lacked proper longitudinal data and comparison groups to adequately show the increased value of such programs. Pharmacy-based interventions focused on increased PrEP uptake should include control groups in order to assess the true effectiveness of these programs in comparison to pre-intervention individuals. They should also be geographically targeted to regions of the country that have populations at high risk for HIV and higher incidence of HIV infection, such as the U.S. Deep South, as well as regions in which pharmacists lack sufficient PrEP knowledge. Pharmacy-based telemedicine interventions may be useful, especially within communities that have difficulty attending appointments with providers, and in the COVID-19 era.

Effective pharmacy-based PrEP interventions require that pharmacists be properly trained on PrEP prescription and adherence [35, 78, 80, 87, 88, 91, 97] . Funding related to the EHE initiative through the CDC HIV Prevention Capacity Building Assistance Program now has specific modules to train pharmacists and pharmacy leadership to integrate expanded communicable diseases testing with provision of PrEP. Comprehensive training of pharmacists, particularly the more experienced, could heighten their willingness to participate in PrEP-related interventions, including screening and identification of eligible individuals. Moreover, adequate PrEP training among pharmacy staff could potentially increase patient comfortability with PrEP prescription and counseling by pharmacists [46, 89] . Following proper training, pharmacists could be integrated into PrEP clinics within community pharmacies through which they may conduct PrEP consultations and prescribe PrEP to eligible patients through CPAs. Patients should still be required to have a negative HIV test for continuing qualification for PrEP, which may be conducted by pharmacists, as well as meet all other CDC requirements for PrEP eligibility. Additionally, increased community education about PrEP may aid in the Fig. 2 Geographic visualization of PrEP knowledge among pharmacists in comparison to PrEP uptake and HIV prevalence in the U.S. State and regional percentages represent those of cohorts utilized in the included studies and do not necessarily reflect state-wide and region-wide data. Beneath represented state names are HIV cases per 100,000 residents of respective state and PrEP users per 100,000 resi-dents of respective state (data from AIDSVu). Grid pattern represents states that have legalized pharmacist PrEP prescriptive authority as of June 2021. Stars represent areas in which pharmacist-led PrEP interventions have been piloted. Percentages listed for Nebraska and Iowa reflect a study in which the data from each state were not disaggregated adjustment of patients to care delivered by non-traditional providers. Subsequently, pharmacists could facilitate adherence counseling and monitoring through in-person visits and telemedicine.

These findings may help inform the development of pharmacy-based PrEP interventions, which we recommend should include practices such as collaborative agreements with physicians, prescriptive authority of pharmacists, and pharmacist and pharmacy student training on PrEP eligibility and adherence.

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